Diversity in the internal functional feeding elements of sympatric morphs of Arctic charr (Salvelinus alpinus)

Abstract

The diversity of functional feeding anatomy is particularly impressive in fishes and correlates with various interspecific ecological specializations. Intraspecific polymorphism can manifest in divergent feeding morphology and ecology, often along a benthic-pelagic axis. Arctic charr (Salvelinus alpinus) is a freshwater salmonid known for morphological variation and sympatric polymorphism and in Lake Þingvallavatn, Iceland, four morphs of charr coexist that differ in preferred prey, behaviour, habitat use, and external feeding morphology. We studied variation in six upper and lower jaw bones in adults of these four morphs using geometric morphometrics and univariate statistics. We tested for allometric differences in bone size and shape among morphs, morph effects on bone size and shape, and divergence along the benthic-pelagic axis. We also examined the degree of integration between bone pairs. We found differences in bone size between pelagic and benthic morphs for two bones (dentary and premaxilla). There was clear bone shape divergence along a benthic-pelagic axis in four bones (dentary, articular-angular, premaxilla and maxilla), as well as allometric shape differences between morphs in the dentary. Notably for the dentary, morph explained more shape variation than bone size. Comparatively, benthic morphs possess a compact and taller dentary, with shorter dentary palate, consistent with visible (but less prominent) differences in external morphology. As these morphs emerged in the last 10,000 years, these results indicate rapid functional evolution of specific feeding structures in arctic charr. This sets the stage for studies of the genetics and development of rapid and parallel craniofacial evolution.

Fig 1. External and internal morphology of Þingvallavatn arctic charr ecomorphs.

A) Craniofacial variation; B) Postcranial shape and size variation; C) Primary upper and lower jaw bones studied; D–I) Anatomy of the upper and lower jaw bones with landmarks used to capture shape.

Fig 2. Size and shape allometry of dentary, articular-angular, premaxilla and maxilla (from top to bottom, inset pictures of each bone).

Left panels: relationships between bone size (y) and fork length (x) by morph; Right panels: relationships between bone shape (y) and bone size (x). Inset are the associated shape changes related to each component, grey outlines the mean shape, and black the two extremes for each PC. Shown are values for individuals (open circles) and the predicted values (filled) of regressions for both bone size (CS_bone) vs body size (log_e FL) or bone-shape versus bone-size. Log_e, natural log transformation.

Fig 3

Strong morph effects on shape variation in the lower jaw bones, dentary (top) and articular angular (bottom). For the dentary, size effects were not removed, but effects of size were removed for articular angular (and other bones, see below). PC-plots of specimens and deformation grids show how shape differences by morphs (grey outlines the mean shape and black lines the two extremes for each PC). None of the shape warps are magnified. Each dot represents an individual and the ellipses 95% CI for the distribution by morph (large dot represents the mean for each morph in these dimensions). PC1 and 2 explain 50% and 13% of the variation in dentary, respectively. For the articular angular (bottom) PC1 and 2 explain 37% and 13%.

Fig 4. Pronounced divergence in premaxilla of the upper jaw and subtle changes in maxilla shape.

Size corrected PC-plots of specimens and deformation grids showing how the morphs differ in mean (top) premaxilla and (bottom) maxilla shape (grey outlines the mean shape and black lines the extremes for each PC). None of the warps (are magnified, representation of PC plots and warps as in Fig 3. For premaxilla (top) PC1 and PC2 explain 25% and 14% of the variation respectively. For maxilla (bottom) PC2 and PC3 explain 23% and 10% respectively (PC1 was biased by sampling error, and not depicted).